The regulation of glucose and lipid homeostasis via PLTP as a mediator of BAT-liver communication.


Journal

EMBO reports
ISSN: 1469-3178
Titre abrégé: EMBO Rep
Pays: England
ID NLM: 100963049

Informations de publication

Date de publication:
03 09 2020
Historique:
received: 09 12 2019
revised: 09 06 2020
accepted: 12 06 2020
pubmed: 17 7 2020
medline: 28 4 2021
entrez: 17 7 2020
Statut: ppublish

Résumé

While brown adipose tissue (BAT) is well-recognized for its ability to dissipate energy in the form of heat, recent studies suggest multifaced roles of BAT in the regulation of glucose and lipid homeostasis beyond stimulating thermogenesis. One of the functions involves interorgan communication with metabolic organs, such as the liver, through BAT-derived secretory factors, a.k.a., batokine. However, the identity and the roles of such mediators remain insufficiently understood. Here, we employed proteomics and transcriptomics in human thermogenic adipocytes and identified previously unappreciated batokines, including phospholipid transfer protein (PLTP). We found that increased circulating levels of PLTP, via systemic or BAT-specific overexpression, significantly improve glucose tolerance and insulin sensitivity, increased energy expenditure, and decrease the circulating levels of cholesterol, phospholipids, and sphingolipids. Such changes were accompanied by increased bile acids in the circulation, which in turn enhances glucose uptake and thermogenesis in BAT. Our data suggest that PLTP is a batokine that contributes to the regulation of systemic glucose and lipid homeostasis as a mediator of BAT-liver interorgan communication.

Identifiants

pubmed: 32672883
doi: 10.15252/embr.201949828
pmc: PMC7507062
doi:

Substances chimiques

Lipids 0
Glucose IY9XDZ35W2

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e49828

Subventions

Organisme : Edward Mallinckrodt, Jr. Foundation (EMF)
Pays : International
Organisme : NIDDK NIH HHS
ID : R01 DK108822
Pays : United States
Organisme : Japan Society for the Promotion of Science London (JSPS London)
Pays : International
Organisme : NCRR NIH HHS
ID : M01 RR001271
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK098722
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK020541
Pays : United States
Organisme : Sao Paulo Research Foundation
ID : 2016/03682-3
Pays : International
Organisme : Manpei Suzuki Diabetes Foundation
Pays : International
Organisme : NIDDK NIH HHS
ID : R01 DK097441
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK125281
Pays : United States

Informations de copyright

© 2020 The Authors.

Références

Circ Res. 2013 Jul 5;113(2):167-75
pubmed: 23676183
J Biol Chem. 1997 Sep 26;272(39):24154-8
pubmed: 9305864
J Biol Chem. 2007 Aug 31;282(35):25940-9
pubmed: 17609208
Endocrinology. 2008 Dec;149(12):6018-27
pubmed: 18687777
Cell Metab. 2019 Nov 5;30(5):963-975.e7
pubmed: 31668873
J Clin Invest. 2005 Jun;115(6):1627-35
pubmed: 15902306
Cell Metab. 2012 Mar 7;15(3):395-404
pubmed: 22405074
Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):14912-7
pubmed: 23980144
J Lipid Res. 2000 Feb;41(2):237-44
pubmed: 10681407
Mol Metab. 2017 Mar 30;6(6):611-619
pubmed: 28580291
Curr Opin Pharmacol. 2015 Oct;24:59-67
pubmed: 26291407
Endocrinology. 2007 Feb;148(2):774-81
pubmed: 17068132
Nat Med. 2017 May;23(5):631-637
pubmed: 28346411
Nature. 2017 Feb 23;542(7642):450-455
pubmed: 28199304
J Biol Chem. 2008 Apr 25;283(17):11541-9
pubmed: 18287097
Circulation. 2011 Aug 2;124(5):555-62
pubmed: 21804130
Diabetes. 2014 Dec;63(12):4089-99
pubmed: 25056438
Nucleic Acids Res. 2018 Mar 16;46(5):2699
pubmed: 29425356
Nature. 2006 Jan 26;439(7075):484-9
pubmed: 16400329
Eur J Endocrinol. 2012 Nov;167(5):671-8
pubmed: 22918303
Nat Med. 2017 Dec;23(12):1454-1465
pubmed: 29131158
Genes Dev. 2015 Feb 1;29(3):298-307
pubmed: 25644604
Cell Metab. 2014 Oct 7;20(4):687-95
pubmed: 25295789
Endocrinology. 1996 Feb;137(2):495-503
pubmed: 8593794
Cell Metab. 2014 Nov 4;20(5):703-705
pubmed: 25440051
Trends Endocrinol Metab. 2018 Jan;29(1):31-41
pubmed: 29195686
Nat Rev Endocrinol. 2017 Feb;13(2):79-91
pubmed: 27767036
Nat Genet. 2009 Jan;41(1):56-65
pubmed: 19060906
Biochim Biophys Acta. 1999 Jul 9;1439(1):65-76
pubmed: 10395966
Nat Rev Endocrinol. 2020 Apr;16(4):224-233
pubmed: 32060415
Biochem Biophys Res Commun. 2001 Oct 5;287(4):921-6
pubmed: 11573953
Mol Cell Proteomics. 2018 Dec;17(12):2358-2370
pubmed: 30135203
Nat Med. 2015 Aug;21(8):863-5
pubmed: 26147760
Cell Metab. 2007 Jul;6(1):38-54
pubmed: 17618855
Nature. 2019 Aug;572(7771):614-619
pubmed: 31435015
Mol Cell Biol. 1998 Sep;18(9):5457-64
pubmed: 9710629
. 2020 Sep 3;21(9):e49828
pubmed: 32672883
J Biol Chem. 2001 Jul 13;276(28):25841-7
pubmed: 11342537
J Biol Chem. 2003 Mar 21;278(12):10297-303
pubmed: 12525490
Endocrinology. 2015 Jul;156(7):2461-9
pubmed: 25830704
Circulation. 2011 Oct 11;124(15):1663-72
pubmed: 21931081
Genes Dev. 2008 May 15;22(10):1397-409
pubmed: 18483224
Eur J Clin Invest. 1994 Mar;24(3):188-94
pubmed: 8033953
Biochem J. 2001 Mar 1;354(Pt 2):359-68
pubmed: 11171115
Nature. 2014 Nov 20;515(7527):355-64
pubmed: 25409824
Cell Metab. 2015 Oct 6;22(4):546-59
pubmed: 26445512
Arterioscler Thromb Vasc Biol. 2015 Feb;35(2):316-22
pubmed: 25477345
Cell. 2006 Jan 13;124(1):35-46
pubmed: 16413480
Biochemistry. 2000 Jun 6;39(22):6660-8
pubmed: 10828984
Metabolism. 2016 Jan;65(1):26-35
pubmed: 26683794
J Clin Invest. 2013 Jan;123(1):215-23
pubmed: 23221344
Biochim Biophys Acta. 1995 Aug 24;1258(1):27-34
pubmed: 7654777
Annu Rev Physiol. 2014;76:225-49
pubmed: 24188710
Nat Med. 2015 Apr;21(4):389-94
pubmed: 25774848
Nat Med. 2011 Feb;17(2):200-5
pubmed: 21258337
Biochim Biophys Acta. 1997 Nov 30;1349(3):222-32
pubmed: 9434136
Cell Metab. 2016 Jun 14;23(6):1200-1206
pubmed: 27238638
Diabetes. 2016 May;65(5):1179-89
pubmed: 26718499
Biochim Biophys Acta. 2012 Mar;1821(3):345-57
pubmed: 21736953
Atherosclerosis. 2014 Apr;233(2):359-362
pubmed: 24530763
J Biol Chem. 2013 Feb 15;288(7):4947-56
pubmed: 23283968
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W429-32
pubmed: 17483518
Front Pharmacol. 2015 Oct 31;6:258
pubmed: 26582989
Diabetes. 2009 Jan;58(1):250-9
pubmed: 18840786
PLoS One. 2012;7(4):e34868
pubmed: 22514681
J Biol Chem. 1995 Jul 21;270(29):17133-8
pubmed: 7615508
Diabetologia. 2001 Sep;44(9):1111-7
pubmed: 11596664
Cell Metab. 2014 Oct 7;20(4):678-86
pubmed: 25295788
Nature. 2019 May;569(7755):229-235
pubmed: 31043739
Cell Metab. 2016 Mar 8;23(3):454-66
pubmed: 26876562
Curr Protoc Mol Biol. 2006 Aug;Chapter 29:Unit 29B.2
pubmed: 18265385
Sci Transl Med. 2017 Oct 18;9(412):
pubmed: 29046435
Cell Metab. 2018 Oct 2;28(4):631-643.e3
pubmed: 30078553
Nat Med. 2017 Oct;23(10):1150-1157
pubmed: 28846097
Mol Cell Biol. 2012 Sep;32(17):3452-63
pubmed: 22733994
Nat Rev Endocrinol. 2017 Jan;13(1):26-35
pubmed: 27616452
Nat Med. 2014 Dec;20(12):1436-1443
pubmed: 25401691
Diabetes. 2010 Nov;59(11):2781-9
pubmed: 20682689
Arterioscler Thromb Vasc Biol. 2018 Aug;38(8):1738-1747
pubmed: 29954752
Nat Med. 2007 Nov;13(11):1333-40
pubmed: 17982462
Arteriosclerosis. 1984 Jan-Feb;4(1):49-58
pubmed: 6691846
Methods Mol Biol. 2017;1611:59-73
pubmed: 28451972
J Biol Chem. 1983 Feb 25;258(4):2174-80
pubmed: 6822552
Eur J Endocrinol. 2009 Sep;161(3):397-404
pubmed: 19515791

Auteurs

Carlos H Sponton (CH)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Takashi Hosono (T)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Junki Taura (J)

End-Organ Disease Laboratories, Daiichi-Sankyo Co., Ltd., Tokyo, Japan.

Mark P Jedrychowski (MP)

Department of Cell Biology, Harvard Medical School, Boston, MA, USA.

Takeshi Yoneshiro (T)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Qiang Wang (Q)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Makoto Takahashi (M)

Drug Metabolism & Pharmacokinetics Research Laboratories, Daiichi-Sankyo Co., Ltd., Tokyo, Japan.

Yumi Matsui (Y)

Protein Production Research Group, Biological Research Department, Daiichi-Sankyo RD Novare Co., Ltd., Tokyo, Japan.

Kenji Ikeda (K)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Yasuo Oguri (Y)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Kazuki Tajima (K)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Kosaku Shinoda (K)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Rachana N Pradhan (RN)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Yong Chen (Y)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Zachary Brown (Z)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Lindsay S Roberts (LS)

Departments of Chemistry, Molecular and Cell Biology, and Nutritional Sciences and Toxicology, University of California, Berkeley, Berkeley, CA, USA.

Carl C Ward (CC)

Departments of Chemistry, Molecular and Cell Biology, and Nutritional Sciences and Toxicology, University of California, Berkeley, Berkeley, CA, USA.

Hiroki Taoka (H)

Graduate School of Media and Governance, Keio University, Kanagawa, Japan.

Yoko Yokoyama (Y)

Graduate School of Media and Governance, Keio University, Kanagawa, Japan.

Mitsuhiro Watanabe (M)

Graduate School of Media and Governance, Keio University, Kanagawa, Japan.

Hiroshi Karasawa (H)

End-Organ Disease Laboratories, Daiichi-Sankyo Co., Ltd., Tokyo, Japan.

Daniel K Nomura (DK)

Departments of Chemistry, Molecular and Cell Biology, and Nutritional Sciences and Toxicology, University of California, Berkeley, Berkeley, CA, USA.

Shingo Kajimura (S)

Diabetes Center, University of California, San Francisco, CA, USA.
Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, San Francisco, CA, USA.
Department of Cell and Tissue Biology, University of California, San Francisco, CA, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH